BREAST SURGERY
Body Mass Index as a Continuous Predictor of Outcomes After Expander-Implant Breast Reconstruction Khang T. Nguyen, BA,* Philip J. Hanwright, BS,* John T. Smetona, BS,* Elliot M. Hirsch, MD,*Þ Akhil K. Seth, MD,*Þ and John Y.S. Kim, MD*Þ Background: Studies show that obesity is a risk factor for complications after expander/implant breast reconstructions. However, reports vary on the precise threshold of body mass index (BMI) as a predictor of heightened risk. We endeavored to link BMI as a continuous variable to overall complications in a single-surgeon series of expander-implant reconstructions. Methods: From 399 patients undergoing expander-implant reconstruction, 551 breasts were stratified to normal weight, overweight, and obese groups for analysis and comparison with previous studies. Logistic regression was performed to predict changes to risk profile per increment of BMI. Results: Complication rates for obese and overweight patients were significantly greater than for normal weight patients, that is, 21.1% and 24.0% versus 10.4%, respectively (P G 0.005). A unit increase in BMI predicted a 5.9% increase in the odds of a complication occurring, and 7.9% increase in the odds of reconstruction ending in failure. Conclusions: By expanding the analysis of BMI to include patients who do not meet the traditional definition of obesity (BMI Q 30 kg/m2), we demonstrated that simply overweight patients (25 e BMI G 30 kg/m2) had an elevated complication rate. Moreover, through regression analysis, we established that BMI as a continuous variable predicts outcomes from expander-based breast reconstruction. Key Words: body mass index, obesity, tissue expander, implant, breast reconstruction, complications, outcomes (Ann Plast Surg 2014;73: 19Y24)
O
besity has a significant impact on reconstructive outcomes for breast cancer patients. It is associated with a poorer prognosis for breast malignancy,1,2 noncancer-related comorbidity and mortality,3Y5 and an increased risk of surgical complications.6Y9 Additionally, obesity may influence the surgeon’s choice of reconstructive method. Previous studies have shown an association between obesity and increased risk of complications in autologous reconstructions,10Y15 leaving some surgeons to prefer tissue expander-based reconstruction for patients with an elevated body mass index (BMI). A smaller body of evidence suggests that obesity may also be predictive of complications after expander-implant reconstructions,.16Y19 However, the existing literature has relied almost exclusively on a binary comparison of obese and nonobese patients, often differentiated at a cutoff BMI of 30 kg/m2 (but occasionally at arbitrary levels). Although this simplifies the analysis, it overlooks the fact that patients fit into a broad Received July 29, 2012, and accepted for publication, after revision, September 28, 2012. From the *Division of Plastic and Reconstructive Surgery, Feinberg School of Medicine, Northwestern University; and †Northwestern Memorial Hospital, Chicago, IL. Conflicts of interest and sources of funding: Dr Kim receives research funding from and is a consultant for the Musculoskeletal Transplant Foundation and Mentor. The remaining authors have nothing to disclose. Reprints: John Yah-Sung Kim, MD, Division of Plastic and Reconstructive Surgery, Feinberg School of Medicine, Northwestern University, 675 N St Clair St, Galter Suite 19-250, Chicago, IL 60611. E-mail: [email protected]. Copyright * 2014 by Lippincott Williams & Wilkins ISSN: 0148-7043/14/7301-0019 DOI: 10.1097/SAP.0b013e318276d91d
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range of BMI, which may allow BMI to be a valuable continuous predictor variable for complications after breast reconstruction. In this study, we conducted a retrospective review of a large cohort of patients who underwent tissue expander-implant breast reconstruction to further evaluate the relationship between BMI and complications in this setting. We performed a stratified analysis of patients based on conventional definitions of being ‘‘overweight’’ and ‘‘obese’’ to facilitate comparison with the existing literature. In addition, we used a regression analysis of BMI as a predictor of complications and reconstructive failure, to add much needed information for a broad spectrum of patients typically defined as nonobese.
PATIENTS AND METHODS Demographic and outcomes data were collected on 551 breasts in 399 patients under the auspices of the institutional review board. Data were based on a consecutive single-surgeon series from August 2004 to May 2012. Age, BMI, smoking status, history of prior radiotherapy, postmastectomy radiotherapy (PXRT), adjuvant chemotherapy, and adjunct acellular dermal matrix (ADM) use in reconstruction were tracked for as covariates. The primary end point was complication at any stage in the reconstructive process, and included mastectomy flap necrosis requiring surgical debridement, tissue expander rupture, infection requiring IV antibiotics, hematoma requiring surgical evacuation, seroma requiring drainage, and wound dehiscence requiring primary or secondary closure. The secondary end point was reoperation due to complications. Specifically, tissue expander explantation and subsequent exchange, conversion to autologous reconstruction, or failure of reconstruction were recorded to evaluate the impact of complications on reconstructive success. For stratified analysis, reconstructed breasts were divided into 3 groups based on patient’s BMI, that is, normal weight (BMI G 25 kg/m2), overweight (25 e BMI G 30 kg/m2), and obese (BMI Q 30 kg/m2). Analysis of variance, Fisher exact probability, and W2 were used as deemed appropriate to compare groups. Alternately, multivariate logistic regression was used to model BMI as a continuous predictor of complications and reoperation while controlling for covariates listed previously which may have been unevenly distributed across groups with traditionally used stratified analysis.
RESULTS Of 551 breasts meeting inclusion criteria, 222, 154, and 175 were stratified to normal weight, overweight, and obese groups, respectively, based on their recorded BMI at the time of surgery. Mean follow-up time was 85.2 (5.9Y201.7) weeks. Demographic and oncologic characteristics of each group are shown in Table 1. Statistically significant differences in mean age, BMI, chemotherapy status, and ADM use existed among groups (P G 0.05 for all). The proportions of active smokers and breasts with prior radiotherapy or PXRT were not significantly different among groups. Rates of complication by group are shown in Table 2. Differences in the rates of overall complications, infections, and seromas were shown to exist among groups. There were no statistically significant differences in the rates of mastectomy flap necrosis, tissue expander rupture, hematoma, and wound dehiscence among groups. www.annalsplasticsurgery.com
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TABLE 1. Demographic and Oncologic Characteristics by Group Normal Weight
Overweight
Obese
TABLE 3. Post Hoc Pairwise Analysis of Group Complication Rates P
Breasts (n) 222 154 175 V Age, mean (SD), y 48 (13.1) 50.1 (12.7) 53.3 (10.6) G0.0001 BMI, mean (SD), kg/m2 22.2 (1.8) 27.3 (1.6) 35.9 (4.9) G0.0001 Active smoker (%) 23 (10.36) 19 (12.34) 11 (6.29) 0.1580 PMRT (%) 48 (21.62) 28 (18.18) 51 (29.14) 0.0502 Prior XRT (%) 16 (7.21) 15 (9.70) 14 (8.00) 0.6737 Chemotherapy (%) 86 (38.74) 72 (46.70) 89 (50.86) 0.0466 ADM (%) 83 (37.39) 88 (57.14) 111 (62.86) G0.0001
Post hoc pairwise comparisons were performed for outcomes with significant differences among groups and are shown in Table 3 and Figure 1. Bonferroni correction was used to determine an acceptable level of significance for post hoc analysis (> = 0.0167). Overweight and obese groups had higher rates of overall complications and infections compared to the normal weight group (P G 0.005 for both). The rate of seroma was only significantly different between normal weight and obese groups (P G 0.01), but not between normal weight and overweight groups. The rates of all categories of complications, and overall complications, were similar between overweight and obese groups. Multivariate logistic regression was performed to determine the relationship between BMI and complications and to eliminate the effect of potential confounding variables that were not evenly distributed among groups in stratified analysis. Body mass index, active smoking status, and PXRT were all significant predictors of overall complications (P G 0.01 for all). Acellular dermal matrix use, chemotherapy, and prior XRT were not significant predictors of overall complications. However, BMI, prior XRT, and ADM use were significant predictors of mastectomy flap necrosis (P G 0.05 for all). Body mass index alone was a significant predictor of infection and seroma (P G 0.01 for both). No variables were found to be associated with tissue expander rupture, hematoma, or wound dehiscence. Odds ratios are presented in Table 4. The overall rate of tissue expander explantation due to complications and rates of successful reconstruction with subsequent expander exchange, conversion to autologous reconstruction, or ultimate failure of reconstruction are shown in Table 5. There were no differences in the rates of tissue expander explantation, expander exchange, autologous salvage, or failure of reconstruction among groups. Multivariate logistic regression indicated that BMI and ADM use were significantly associated with tissue expander explantation due to complications (P G 0.05). Body mass index was also
TABLE 2. Complications by Group Normal Weight Overweight Overall complications (%) 22 (9.91) Mastectomy flap necrosis (%) 9 (4.05) Tissue expander rupture (%) 3 (1.35) Infection (%) 5 (2.25) Hematoma (%) 4 (1.80) Seroma (%) 3 (1.35) Dehiscence (%) 13 (5.86)
20
36 11 1 14 4 5 15
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(23.34) (7.14) (0.65) (9.09) (2.60) (3.25) (9.74)
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Obese
P
36 (20.57) 16 (9.14) 5 (2.86) 13 (7.43) 3 (1.71) 11 (6.29) 12 (6.86)
0.00103 0.1177 0.2632 0.0111 0.8138 0.0276 0.3499
Complication Overall complications Mastectomy flap necrosis Infection Seroma
Normal Weight Versus Overweight (P)
Normal Weight Versus Obese (P)
Overweight Versus Obese (P)
0.0005
0.0039
0.5937
0.1894
0.0382
0.4877
0.0029 0.2104
0.0138 0.0081
0.5096 0.2010
Tissue expander rupture, hematoma, and dehiscence were not included in pairwise analysis due to lack of significance on W2 and logistic regression for association with BMI. Bonferroni correction was used to determine an acceptable level of significance for post hoc analysis (> = 0.0166).
associated with subsequent expander exchange and ultimate failure of reconstruction (P G 0.05 for both). Odds ratios are presented in Table 6.
DISCUSSION The association between obesity and complications after autologous breast reconstruction has been widely documented.10Y14,20 Studies have also identified obesity as a risk factor for complications after expander-implant reconstructions.16Y19 However, this volume of evidence is more modest. Additionally, few reports have performed a dedicated evaluation of BMI as a continuous predictor of complications, which may provide valuable information for patients traditionally categorized as ‘‘nonobese.’’ McCarthy et al16 found that BMI greater than or equal to 30 kg/m2 was a significant predictor of overall complications and reconstructive failure in a large cohort of expander-implant reconstructions with a significant follow-up period. Woerderman et al19 found that a BMI greater than 24 kg/m2 was significantly associated with implant failure but, surprisingly, not with overall complications in a mixed cohort of expander-implant or immediate implant reconstructions. Although a cutoff BMI of 24 kg/m2 is more inclusive of patients with moderate BMI, it also raises concerns, as this neither meets the traditionally accepted definition of obesity (BMI Q 30 kg/m2) nor overweight status (25 e BMI G 30 kg/m2), and does not provide information on differences between such populations. In contrast, Alderman et al17 used BMI as a continuous variable. They showed that it was a predictor of overall complications and major complications (those requiring inpatient intervention) in a mixed cohort of expander-implant and autologous reconstructions, but did not evaluate BMI as a predictor of individual categories of complications or overall complications in expander-implants reconstructions alone. Consistent with these reports, we found that obese patients experienced higher complication rates compared to normal weight patients. Interestingly, we also found that overweight patients also had higher complication rates than normal weight patients. In fact, overweight patients and obese patients had similar rates of overall complications as well as similar rates of all individual categories of complications. This is the first direct comparison of complication rates for overweight and obese patients, as overweight patients typically fell into the nonobese category in most of other analyses or were grouped with obese patients in the rare instance discussed previously. Analysis by individual categories of complications revealed that obese and overweight patients experienced significantly greater rates of infections. Previous studies have examined risk factors for * 2014 Lippincott Williams & Wilkins
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BMI and Expander-Implant Breast Reconstructions
FIGURE 1. Bar graph of complication profiles by BMI strata. W2 and post hoc pairwise analysis were performed. Bonferroni correction was used to determine an acceptable level of significance for post hoc analysis (> = 0.0167). *P G 0.0167; **P G 0.005.
infection in tissue expander reconstructions with inconclusive results. Olsen et al21 found a significant association between patients with BMI greater than or equal to 35 kg/m2 and increased risk of infection in a retrospective review of surgical site infections after major breast surgery. However, they found no statistically significant association between overweight patients or obese patients with BMI less than 35 kg/m2 and increased risk of infection. This may have stemmed from the heterogeneity of procedures allowed by their inclusion criteria. Likewise, Francis et al22 found no association between BMI and infection in large cohort of expander-based reconstructions. Still others either did not look at BMI or obesity or were limited by small sample size.18,23,24 W2 also revealed a difference among groups in the rate of seromas, but there was only a statistically significant difference between obese and normal weight groups on pairwise comparison. The rate of seromas in overweight patients was between that of normal weight and obese patients, suggesting a linear association with BMI, while obscuring more subtle differences in conservative post hoc pairwise comparison of overweight and normal weight groups. As such, multivariate logistic regression was performed and revealed that a unit increase in BMI was significantly associated with 5.23% increase in the odds of complications overall, 8.20% increase in the odds of infection, 9.23% increase in the odds of seroma, and 5.21% increase in the odds of mastectomy flap necrosis. Explanations have been proposed for the association between obesity and these specific complications. It has been hypothesized that tissue flaps in obese patients tend to be heavy and large, leading to stretching and compression of perforators as well as a greater volume of tissue being dependent on limited vascular supply.25,26 Poor perfusion of the distal edges of reconstructive flaps may contribute to higher rates of infection and necrosis. Likewise, dead space formed by abundant, poorly perfused adipose tissue may also contribute to seroma formation in patients with very high BMI.27 This may be especially true for autologous reconstructions. The senior author has adopted the use of quilting sutures to secure cutaneous * 2014 Lippincott Williams & Wilkins
flaps against the body wall to minimize dead-space formation.28 In obese patients who undergo mastectomy followed by tissue expander placement, perfusion defects may result from both longer flaps and from the propensity to overexpand the patient’s larger area of mastectomy flaps. Indeed, an association between large intraoperative tissue expander fill volumes and mastectomy flap necrosis has been noted.15 In addition to dead space due to the mastectomy defect, shearing between the mastectomy flaps and an actively expanded pectoralis may lead to seroma formation.29,30 To determine the impact of complications on the reconstructive process, we identified cases of tissue expander explantation resulting from complications and determined whether they successfully completed reconstruction with expander exchange or conversion to autologous flaps, or ultimately failed to complete reconstruction. Logistic regression indicated that a unit increase in BMI was significant associated with a 4.28% increase in the odds of tissue expander explantation. Body mass index was not predictive of conversion to autologous reconstruction, but a unit increase in BMI was associated with an 8.72% increase in the odds of expander exchange and 6.99% increase in the odds of ultimate reconstructive failure. Patient and surgeon preference may heavily influence the next step in reconstruction after initial tissue expander explantation, potentially affecting the association between BMI and success in one salvage method versus another. Likewise, we did not determine whether patients and the plastic surgeon exhausted all available salvage procedures before choosing to abort the reconstructive process, which introduces another potential confounder in this analysis. Additionally, active smoking status and PXRT were also significant independent predictors of overall complications. These risk factors are well established in the literature.18,22,31,32 However, these variables were not significantly associated with the tissue expander explantation and exchange, conversion to autologous reconstruction, or failure of reconstruction. Acellular dermal matrix use was not significantly associated with overall complications in our study. The use of ADM to provide www.annalsplasticsurgery.com
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TABLE 4. Multivariate Logistic Regression of Risk Factors for Complications Risk Factor Overall complications Age BMI, kg/m2 Active smoker Prior XRT Chemotherapy PXRT ADM Mastectomy flap necrosis Age BMI, kg/m2 Active smoker Prior XRT Chemotherapy PXRT ADM Tissue expander rupture Age BMI Active smoker Prior XRT Chemotherapy PXRT ADM Infection Age BMI, kg/m2 Active smoker Prior XRT Chemotherapy PXRT ADM Hematoma Age BMI Active smoker Prior XRT Chemotherapy PXRT ADM Seroma Age BMI Active smoker Prior XRT Chemotherapy PXRT ADM Dehiscence Age BMI Active smoker Prior XRT Chemotherapy PXRT ADM
22
Odds Ratio (95% Confidence Interval)
P
V 1.0529 (1.0188Y1.0882) 2.5709 (1.3160Y5.0227) V V 3.3542 (1.9173Y5.8681) V
0.8281 0.0022 0.0057 0.5411 0.3748 G0.0001 0.4028
V 1.0521 (1.0015Y1.1052) V 3.1219 (1.2250Y7.9562) V V 2.2327 (1.0191Y4.8914)
0.0996 0.0434 0.0606 0.0171 0.6663 0.4941 0.0447
V V V V V V V
0.5073 0.4490 0.9981 0.8720 0.9341 0.4601 0.2279
V 1.0817 (1.0319Y1.1340) V V V V V
0.5812 0.0011 0.2286 0.6393 0.4131 0.5772 0.8513
V V V V V V V
0.2225 0.8777 0.9526 0.9980 0.6102 0.8733 0.4406
V 1.0923 (1.0320Y1.1562) V V V V V
0.9912 0.0023 0.5793 0.7182 0.4782 0.7961 0.3297
V V V V V V V
0.8263 0.6015 0.8642 0.8622 0.5687 0.5772 0.8806
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improved subpectoral coverage of prostheses in expander-implant reconstructions has gained enormous popularity with plastic surgeons.28,33,34 Importantly, some surgeons have favored this technique for patients with high BMI or large prostheses.28,35,36 There has been significant controversy regarding potential associations between ADM use and increased rates of complications.35,37Y40 A recent meta-analysis of 19 studies suggests that ADM use may increase rates of complications.41 Nevertheless, the magnitudes of these differences may be acceptably small.41 We found that ADM use was significantly associated with a 2.23-fold increase in the odds of mastectomy flap necrosis, but was also associated with a 57% decrease in the odds of tissue expander explantation. Interestingly, multivariate logistic regression revealed a number of limitations associated with stratified analysis, including the inability to correct for potential confounding variables that were unevenly distributed among groups (ie, ADM use and chemotherapy) and poor sensitivity in detecting differences in the rates of mastectomy flap necrosis, expander explantations, expander exchanges, and reconstructive failure among groups. This suggests that transformation of BMI into a categorical variable may obscure some of its predictive value for outcomes in breast reconstruction. Although logistic regression is often performed after conversion of BMI data into an obese versus nonobese dichotomy to eliminate confounders, we have shown that information on overweight patients may still be overlooked with this method. Furthermore, inconsistent grouping of patients with intermediate BMI, such as overweight patients, with either obese or normal weight patients in the existing literature may affect findings. Recently, Momeni et al42 have questioned the paradigm of avoiding autologous reconstructions for obese patients, and as a corollary, whether expander-implant reconstructions should remain the alternative for these patients. Their retrospective review of 42 autologous reconstructions revealed a 32.1% complication rate in patients with BMI greater than or equal to 35 kg/m2 and Jandali et al14 and Momeni et al42 found a 72% complication rate for autologous reconstructions in patients with BMI greater than or equal to 40 kg/m2. In the present study, overweight and obese patients undergoing expander-implant reconstructions had 23.72% and 21.14% overall complication rates, respectively. Although it superficially seems that autologous reconstruction may lead to higher complication rates in these populations, attempts at cross-study comparisons are challenging due to variations in definition of complications and arbitrary BMI cutoffs for stratification. Additionally, the question of how to differentiate betweenVand attribute risk toVmorbidly obese and obese patients remains unaddressed. These inconsistencies further support the practicality of using the universally defined BMI statistic as a continuous predictor variable of complications instead of transforming this information into dichotomies for analysis. Limitations to the validity of BMI as a continuous predictor for complications in breast reconstruction include potentially abnormal predictive behavior of extreme BMI. Extremely underweight or
TABLE 5. Reoperations Due to Complications by Group Normal Weight Overweight Tissue expander 21 (9.46) explantation (%) Tissue expander exchange (%) 1 (0.45) Conversion to autologous 17 (4.05) reconstruction (%) Reconstruction failure (%) 3 (1.35)
Obese
P
20 (12.87)
23 (13.14) 0.4396
3 (1.95) 10 (7.14)
3 (1.71) 12 (9.14)
0.8138 0.5916
7 (4.55)
8 (4.57)
0.1153
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TABLE 6. Multivariate Regression of Risk Factors for Reoperation Due to Complications Odds Ratio (95% Confidence Interval)
P
V 1.0428 (1.0036Y1.0836) V V V V 0.4269 (0.2406Y0.7574)
0.1375 0.0322 0.8643 0.3067 0.3987 0.4278 0.0036
V 1.0872 (1.0014Y1.1803) V V V V V
0.6719 0.0463 0.9987 0.9988 0.9457 0.4348 0.4857
V V V V V V V
0.1109 0.9388 0.4398 0.5005 0.5550 0.4315 0.0587
V 1.0699 (1.0064Y1.1374) V V V V V
0.5192 0.0305 0.4222 0.7343 0.3029 0.4112 0.1083
Risk Factor Tissue explantation Age BMI, kg/m2 Active smoker Prior XRT Chemotherapy PXRT ADM Tissue expander exchange Age BMI, kg/m2 Active smoker Prior XRT Chemotherapy PXRT ADM Conversion to autologous reconstruction Age BMI Active smoker Prior XRT Chemotherapy PXRT ADM Reconstruction failure Age BMI, kg/m2 Active smoker Prior XRT Chemotherapy PXRT ADM
morbidly obese patients may both experience comorbidities that drastically affect surgical outcomes. Nevertheless, in those circumstances, coexisting medical concerns clearly outweigh BMI in guiding the decision to undergo reconstruction.
CONCLUSIONS This study evaluates BMI as a continuous variable predictor of complications in tissue expander-implant breast reconstructions. Stratification of patients into obese and nonobese risk groups, as is customary in the existing literature, may not adequately estimate risk for patients. By considering BMI rather than obesity, plastic surgeons may better predict outcomes and guide patient care. REFERENCES 1. Demark-Wahnefried W, Campbell KL, Hayes SC. Weight management and its role in breast cancer rehabilitation. Cancer. 2012;118(suppl 8):2277Y2287. 2. Cleary MP, Grossmann ME. Minireview: Obesity and breast cancer: the estrogen connection. Endocrinology. 2009;150:2537Y2542. 3. Calle EE, Thun MJ, Petrelli JM, et al. Body-mass index and mortality in a prospective cohort of U.S. adults. N Engl J Med. 1999;341:1097Y1105. 4. Burton BT, Foster WR, Hirsch J, et al. Health implications of obesity: an NIH Consensus Development Conference. Int J Obes. 1985;9:155Y170.
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BMI and Expander-Implant Breast Reconstructions
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36. Maxwell GP, Gabriel A. Use of the acellular dermal matrix in revisionary aesthetic breast surgery. Aesthet Surg J. 2009;29:485Y493. 37. Rawlani V, Buck DW 2nd, Johnson SA, et al. Tissue expander breast reconstruction using prehydrated human acellular dermis. Ann Plast Surg. 2011;66: 593Y597. 38. Chun YS, Verma K, Rosen H, et al. Implant-based breast reconstruction using acellular dermal matrix and the risk of postoperative complications. Plast Reconstr Surg. 2010;125:429Y436. 39. Antony AK, McCarthy CM, Cordeiro PG, et al. Acellular human dermis implantation in 153 immediate two-stage tissue expander breast reconstructions:
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determining the incidence and significant predictors of complications. Plast Reconstr Surg. 2010;125:1606Y1614. 40. Sbitany H, Serletti JM. Acellular dermis-assisted prosthetic breast reconstruction: a systematic and critical review of efficacy and associated morbidity. Plast Reconstr Surg. 2011;128:1162Y1169. 41. Kim JY, Davila AA, Persing S, et al. A meta-analysis of human acellular dermis and submuscular tissue expander breast reconstruction. Plast Reconstr Surg. 2012;129:28Y41. 42. Momeni A, Ahdoot MA, Kim RY, et al. Should we continue to consider obesity a relative contraindication for autologous microsurgical breast reconstruction? J Plast Reconstr Aesthet Surg. 2012;65:420Y425.
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Body Mass Index as a Continuous Predictor of Outcomes After Expander-Implant Breast Reconstruction Khang T. Nguyen, BA,* Philip J. Hanwright, BS,* John T. Smetona, BS,* Elliot M. Hirsch, MD,*Þ Akhil K. Seth, MD,*Þ and John Y.S. Kim, MD*Þ Background: Studies show that obesity is a risk factor for complications after expander/implant breast reconstructions. However, reports vary on the precise threshold of body mass index (BMI) as a predictor of heightened risk. We endeavored to link BMI as a continuous variable to overall complications in a single-surgeon series of expander-implant reconstructions. Methods: From 399 patients undergoing expander-implant reconstruction, 551 breasts were stratified to normal weight, overweight, and obese groups for analysis and comparison with previous studies. Logistic regression was performed to predict changes to risk profile per increment of BMI. Results: Complication rates for obese and overweight patients were significantly greater than for normal weight patients, that is, 21.1% and 24.0% versus 10.4%, respectively (P G 0.005). A unit increase in BMI predicted a 5.9% increase in the odds of a complication occurring, and 7.9% increase in the odds of reconstruction ending in failure. Conclusions: By expanding the analysis of BMI to include patients who do not meet the traditional definition of obesity (BMI Q 30 kg/m2), we demonstrated that simply overweight patients (25 e BMI G 30 kg/m2) had an elevated complication rate. Moreover, through regression analysis, we established that BMI as a continuous variable predicts outcomes from expander-based breast reconstruction. Key Words: body mass index, obesity, tissue expander, implant, breast reconstruction, complications, outcomes (Ann Plast Surg 2014;73: 19Y24)
O
besity has a significant impact on reconstructive outcomes for breast cancer patients. It is associated with a poorer prognosis for breast malignancy,1,2 noncancer-related comorbidity and mortality,3Y5 and an increased risk of surgical complications.6Y9 Additionally, obesity may influence the surgeon’s choice of reconstructive method. Previous studies have shown an association between obesity and increased risk of complications in autologous reconstructions,10Y15 leaving some surgeons to prefer tissue expander-based reconstruction for patients with an elevated body mass index (BMI). A smaller body of evidence suggests that obesity may also be predictive of complications after expander-implant reconstructions,.16Y19 However, the existing literature has relied almost exclusively on a binary comparison of obese and nonobese patients, often differentiated at a cutoff BMI of 30 kg/m2 (but occasionally at arbitrary levels). Although this simplifies the analysis, it overlooks the fact that patients fit into a broad Received July 29, 2012, and accepted for publication, after revision, September 28, 2012. From the *Division of Plastic and Reconstructive Surgery, Feinberg School of Medicine, Northwestern University; and †Northwestern Memorial Hospital, Chicago, IL. Conflicts of interest and sources of funding: Dr Kim receives research funding from and is a consultant for the Musculoskeletal Transplant Foundation and Mentor. The remaining authors have nothing to disclose. Reprints: John Yah-Sung Kim, MD, Division of Plastic and Reconstructive Surgery, Feinberg School of Medicine, Northwestern University, 675 N St Clair St, Galter Suite 19-250, Chicago, IL 60611. E-mail: [email protected]. Copyright * 2014 by Lippincott Williams & Wilkins ISSN: 0148-7043/14/7301-0019 DOI: 10.1097/SAP.0b013e318276d91d
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range of BMI, which may allow BMI to be a valuable continuous predictor variable for complications after breast reconstruction. In this study, we conducted a retrospective review of a large cohort of patients who underwent tissue expander-implant breast reconstruction to further evaluate the relationship between BMI and complications in this setting. We performed a stratified analysis of patients based on conventional definitions of being ‘‘overweight’’ and ‘‘obese’’ to facilitate comparison with the existing literature. In addition, we used a regression analysis of BMI as a predictor of complications and reconstructive failure, to add much needed information for a broad spectrum of patients typically defined as nonobese.
PATIENTS AND METHODS Demographic and outcomes data were collected on 551 breasts in 399 patients under the auspices of the institutional review board. Data were based on a consecutive single-surgeon series from August 2004 to May 2012. Age, BMI, smoking status, history of prior radiotherapy, postmastectomy radiotherapy (PXRT), adjuvant chemotherapy, and adjunct acellular dermal matrix (ADM) use in reconstruction were tracked for as covariates. The primary end point was complication at any stage in the reconstructive process, and included mastectomy flap necrosis requiring surgical debridement, tissue expander rupture, infection requiring IV antibiotics, hematoma requiring surgical evacuation, seroma requiring drainage, and wound dehiscence requiring primary or secondary closure. The secondary end point was reoperation due to complications. Specifically, tissue expander explantation and subsequent exchange, conversion to autologous reconstruction, or failure of reconstruction were recorded to evaluate the impact of complications on reconstructive success. For stratified analysis, reconstructed breasts were divided into 3 groups based on patient’s BMI, that is, normal weight (BMI G 25 kg/m2), overweight (25 e BMI G 30 kg/m2), and obese (BMI Q 30 kg/m2). Analysis of variance, Fisher exact probability, and W2 were used as deemed appropriate to compare groups. Alternately, multivariate logistic regression was used to model BMI as a continuous predictor of complications and reoperation while controlling for covariates listed previously which may have been unevenly distributed across groups with traditionally used stratified analysis.
RESULTS Of 551 breasts meeting inclusion criteria, 222, 154, and 175 were stratified to normal weight, overweight, and obese groups, respectively, based on their recorded BMI at the time of surgery. Mean follow-up time was 85.2 (5.9Y201.7) weeks. Demographic and oncologic characteristics of each group are shown in Table 1. Statistically significant differences in mean age, BMI, chemotherapy status, and ADM use existed among groups (P G 0.05 for all). The proportions of active smokers and breasts with prior radiotherapy or PXRT were not significantly different among groups. Rates of complication by group are shown in Table 2. Differences in the rates of overall complications, infections, and seromas were shown to exist among groups. There were no statistically significant differences in the rates of mastectomy flap necrosis, tissue expander rupture, hematoma, and wound dehiscence among groups. www.annalsplasticsurgery.com
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TABLE 1. Demographic and Oncologic Characteristics by Group Normal Weight
Overweight
Obese
TABLE 3. Post Hoc Pairwise Analysis of Group Complication Rates P
Breasts (n) 222 154 175 V Age, mean (SD), y 48 (13.1) 50.1 (12.7) 53.3 (10.6) G0.0001 BMI, mean (SD), kg/m2 22.2 (1.8) 27.3 (1.6) 35.9 (4.9) G0.0001 Active smoker (%) 23 (10.36) 19 (12.34) 11 (6.29) 0.1580 PMRT (%) 48 (21.62) 28 (18.18) 51 (29.14) 0.0502 Prior XRT (%) 16 (7.21) 15 (9.70) 14 (8.00) 0.6737 Chemotherapy (%) 86 (38.74) 72 (46.70) 89 (50.86) 0.0466 ADM (%) 83 (37.39) 88 (57.14) 111 (62.86) G0.0001
Post hoc pairwise comparisons were performed for outcomes with significant differences among groups and are shown in Table 3 and Figure 1. Bonferroni correction was used to determine an acceptable level of significance for post hoc analysis (> = 0.0167). Overweight and obese groups had higher rates of overall complications and infections compared to the normal weight group (P G 0.005 for both). The rate of seroma was only significantly different between normal weight and obese groups (P G 0.01), but not between normal weight and overweight groups. The rates of all categories of complications, and overall complications, were similar between overweight and obese groups. Multivariate logistic regression was performed to determine the relationship between BMI and complications and to eliminate the effect of potential confounding variables that were not evenly distributed among groups in stratified analysis. Body mass index, active smoking status, and PXRT were all significant predictors of overall complications (P G 0.01 for all). Acellular dermal matrix use, chemotherapy, and prior XRT were not significant predictors of overall complications. However, BMI, prior XRT, and ADM use were significant predictors of mastectomy flap necrosis (P G 0.05 for all). Body mass index alone was a significant predictor of infection and seroma (P G 0.01 for both). No variables were found to be associated with tissue expander rupture, hematoma, or wound dehiscence. Odds ratios are presented in Table 4. The overall rate of tissue expander explantation due to complications and rates of successful reconstruction with subsequent expander exchange, conversion to autologous reconstruction, or ultimate failure of reconstruction are shown in Table 5. There were no differences in the rates of tissue expander explantation, expander exchange, autologous salvage, or failure of reconstruction among groups. Multivariate logistic regression indicated that BMI and ADM use were significantly associated with tissue expander explantation due to complications (P G 0.05). Body mass index was also
TABLE 2. Complications by Group Normal Weight Overweight Overall complications (%) 22 (9.91) Mastectomy flap necrosis (%) 9 (4.05) Tissue expander rupture (%) 3 (1.35) Infection (%) 5 (2.25) Hematoma (%) 4 (1.80) Seroma (%) 3 (1.35) Dehiscence (%) 13 (5.86)
20
36 11 1 14 4 5 15
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(23.34) (7.14) (0.65) (9.09) (2.60) (3.25) (9.74)
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Obese
P
36 (20.57) 16 (9.14) 5 (2.86) 13 (7.43) 3 (1.71) 11 (6.29) 12 (6.86)
0.00103 0.1177 0.2632 0.0111 0.8138 0.0276 0.3499
Complication Overall complications Mastectomy flap necrosis Infection Seroma
Normal Weight Versus Overweight (P)
Normal Weight Versus Obese (P)
Overweight Versus Obese (P)
0.0005
0.0039
0.5937
0.1894
0.0382
0.4877
0.0029 0.2104
0.0138 0.0081
0.5096 0.2010
Tissue expander rupture, hematoma, and dehiscence were not included in pairwise analysis due to lack of significance on W2 and logistic regression for association with BMI. Bonferroni correction was used to determine an acceptable level of significance for post hoc analysis (> = 0.0166).
associated with subsequent expander exchange and ultimate failure of reconstruction (P G 0.05 for both). Odds ratios are presented in Table 6.
DISCUSSION The association between obesity and complications after autologous breast reconstruction has been widely documented.10Y14,20 Studies have also identified obesity as a risk factor for complications after expander-implant reconstructions.16Y19 However, this volume of evidence is more modest. Additionally, few reports have performed a dedicated evaluation of BMI as a continuous predictor of complications, which may provide valuable information for patients traditionally categorized as ‘‘nonobese.’’ McCarthy et al16 found that BMI greater than or equal to 30 kg/m2 was a significant predictor of overall complications and reconstructive failure in a large cohort of expander-implant reconstructions with a significant follow-up period. Woerderman et al19 found that a BMI greater than 24 kg/m2 was significantly associated with implant failure but, surprisingly, not with overall complications in a mixed cohort of expander-implant or immediate implant reconstructions. Although a cutoff BMI of 24 kg/m2 is more inclusive of patients with moderate BMI, it also raises concerns, as this neither meets the traditionally accepted definition of obesity (BMI Q 30 kg/m2) nor overweight status (25 e BMI G 30 kg/m2), and does not provide information on differences between such populations. In contrast, Alderman et al17 used BMI as a continuous variable. They showed that it was a predictor of overall complications and major complications (those requiring inpatient intervention) in a mixed cohort of expander-implant and autologous reconstructions, but did not evaluate BMI as a predictor of individual categories of complications or overall complications in expander-implants reconstructions alone. Consistent with these reports, we found that obese patients experienced higher complication rates compared to normal weight patients. Interestingly, we also found that overweight patients also had higher complication rates than normal weight patients. In fact, overweight patients and obese patients had similar rates of overall complications as well as similar rates of all individual categories of complications. This is the first direct comparison of complication rates for overweight and obese patients, as overweight patients typically fell into the nonobese category in most of other analyses or were grouped with obese patients in the rare instance discussed previously. Analysis by individual categories of complications revealed that obese and overweight patients experienced significantly greater rates of infections. Previous studies have examined risk factors for * 2014 Lippincott Williams & Wilkins
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BMI and Expander-Implant Breast Reconstructions
FIGURE 1. Bar graph of complication profiles by BMI strata. W2 and post hoc pairwise analysis were performed. Bonferroni correction was used to determine an acceptable level of significance for post hoc analysis (> = 0.0167). *P G 0.0167; **P G 0.005.
infection in tissue expander reconstructions with inconclusive results. Olsen et al21 found a significant association between patients with BMI greater than or equal to 35 kg/m2 and increased risk of infection in a retrospective review of surgical site infections after major breast surgery. However, they found no statistically significant association between overweight patients or obese patients with BMI less than 35 kg/m2 and increased risk of infection. This may have stemmed from the heterogeneity of procedures allowed by their inclusion criteria. Likewise, Francis et al22 found no association between BMI and infection in large cohort of expander-based reconstructions. Still others either did not look at BMI or obesity or were limited by small sample size.18,23,24 W2 also revealed a difference among groups in the rate of seromas, but there was only a statistically significant difference between obese and normal weight groups on pairwise comparison. The rate of seromas in overweight patients was between that of normal weight and obese patients, suggesting a linear association with BMI, while obscuring more subtle differences in conservative post hoc pairwise comparison of overweight and normal weight groups. As such, multivariate logistic regression was performed and revealed that a unit increase in BMI was significantly associated with 5.23% increase in the odds of complications overall, 8.20% increase in the odds of infection, 9.23% increase in the odds of seroma, and 5.21% increase in the odds of mastectomy flap necrosis. Explanations have been proposed for the association between obesity and these specific complications. It has been hypothesized that tissue flaps in obese patients tend to be heavy and large, leading to stretching and compression of perforators as well as a greater volume of tissue being dependent on limited vascular supply.25,26 Poor perfusion of the distal edges of reconstructive flaps may contribute to higher rates of infection and necrosis. Likewise, dead space formed by abundant, poorly perfused adipose tissue may also contribute to seroma formation in patients with very high BMI.27 This may be especially true for autologous reconstructions. The senior author has adopted the use of quilting sutures to secure cutaneous * 2014 Lippincott Williams & Wilkins
flaps against the body wall to minimize dead-space formation.28 In obese patients who undergo mastectomy followed by tissue expander placement, perfusion defects may result from both longer flaps and from the propensity to overexpand the patient’s larger area of mastectomy flaps. Indeed, an association between large intraoperative tissue expander fill volumes and mastectomy flap necrosis has been noted.15 In addition to dead space due to the mastectomy defect, shearing between the mastectomy flaps and an actively expanded pectoralis may lead to seroma formation.29,30 To determine the impact of complications on the reconstructive process, we identified cases of tissue expander explantation resulting from complications and determined whether they successfully completed reconstruction with expander exchange or conversion to autologous flaps, or ultimately failed to complete reconstruction. Logistic regression indicated that a unit increase in BMI was significant associated with a 4.28% increase in the odds of tissue expander explantation. Body mass index was not predictive of conversion to autologous reconstruction, but a unit increase in BMI was associated with an 8.72% increase in the odds of expander exchange and 6.99% increase in the odds of ultimate reconstructive failure. Patient and surgeon preference may heavily influence the next step in reconstruction after initial tissue expander explantation, potentially affecting the association between BMI and success in one salvage method versus another. Likewise, we did not determine whether patients and the plastic surgeon exhausted all available salvage procedures before choosing to abort the reconstructive process, which introduces another potential confounder in this analysis. Additionally, active smoking status and PXRT were also significant independent predictors of overall complications. These risk factors are well established in the literature.18,22,31,32 However, these variables were not significantly associated with the tissue expander explantation and exchange, conversion to autologous reconstruction, or failure of reconstruction. Acellular dermal matrix use was not significantly associated with overall complications in our study. The use of ADM to provide www.annalsplasticsurgery.com
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TABLE 4. Multivariate Logistic Regression of Risk Factors for Complications Risk Factor Overall complications Age BMI, kg/m2 Active smoker Prior XRT Chemotherapy PXRT ADM Mastectomy flap necrosis Age BMI, kg/m2 Active smoker Prior XRT Chemotherapy PXRT ADM Tissue expander rupture Age BMI Active smoker Prior XRT Chemotherapy PXRT ADM Infection Age BMI, kg/m2 Active smoker Prior XRT Chemotherapy PXRT ADM Hematoma Age BMI Active smoker Prior XRT Chemotherapy PXRT ADM Seroma Age BMI Active smoker Prior XRT Chemotherapy PXRT ADM Dehiscence Age BMI Active smoker Prior XRT Chemotherapy PXRT ADM
22
Odds Ratio (95% Confidence Interval)
P
V 1.0529 (1.0188Y1.0882) 2.5709 (1.3160Y5.0227) V V 3.3542 (1.9173Y5.8681) V
0.8281 0.0022 0.0057 0.5411 0.3748 G0.0001 0.4028
V 1.0521 (1.0015Y1.1052) V 3.1219 (1.2250Y7.9562) V V 2.2327 (1.0191Y4.8914)
0.0996 0.0434 0.0606 0.0171 0.6663 0.4941 0.0447
V V V V V V V
0.5073 0.4490 0.9981 0.8720 0.9341 0.4601 0.2279
V 1.0817 (1.0319Y1.1340) V V V V V
0.5812 0.0011 0.2286 0.6393 0.4131 0.5772 0.8513
V V V V V V V
0.2225 0.8777 0.9526 0.9980 0.6102 0.8733 0.4406
V 1.0923 (1.0320Y1.1562) V V V V V
0.9912 0.0023 0.5793 0.7182 0.4782 0.7961 0.3297
V V V V V V V
0.8263 0.6015 0.8642 0.8622 0.5687 0.5772 0.8806
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improved subpectoral coverage of prostheses in expander-implant reconstructions has gained enormous popularity with plastic surgeons.28,33,34 Importantly, some surgeons have favored this technique for patients with high BMI or large prostheses.28,35,36 There has been significant controversy regarding potential associations between ADM use and increased rates of complications.35,37Y40 A recent meta-analysis of 19 studies suggests that ADM use may increase rates of complications.41 Nevertheless, the magnitudes of these differences may be acceptably small.41 We found that ADM use was significantly associated with a 2.23-fold increase in the odds of mastectomy flap necrosis, but was also associated with a 57% decrease in the odds of tissue expander explantation. Interestingly, multivariate logistic regression revealed a number of limitations associated with stratified analysis, including the inability to correct for potential confounding variables that were unevenly distributed among groups (ie, ADM use and chemotherapy) and poor sensitivity in detecting differences in the rates of mastectomy flap necrosis, expander explantations, expander exchanges, and reconstructive failure among groups. This suggests that transformation of BMI into a categorical variable may obscure some of its predictive value for outcomes in breast reconstruction. Although logistic regression is often performed after conversion of BMI data into an obese versus nonobese dichotomy to eliminate confounders, we have shown that information on overweight patients may still be overlooked with this method. Furthermore, inconsistent grouping of patients with intermediate BMI, such as overweight patients, with either obese or normal weight patients in the existing literature may affect findings. Recently, Momeni et al42 have questioned the paradigm of avoiding autologous reconstructions for obese patients, and as a corollary, whether expander-implant reconstructions should remain the alternative for these patients. Their retrospective review of 42 autologous reconstructions revealed a 32.1% complication rate in patients with BMI greater than or equal to 35 kg/m2 and Jandali et al14 and Momeni et al42 found a 72% complication rate for autologous reconstructions in patients with BMI greater than or equal to 40 kg/m2. In the present study, overweight and obese patients undergoing expander-implant reconstructions had 23.72% and 21.14% overall complication rates, respectively. Although it superficially seems that autologous reconstruction may lead to higher complication rates in these populations, attempts at cross-study comparisons are challenging due to variations in definition of complications and arbitrary BMI cutoffs for stratification. Additionally, the question of how to differentiate betweenVand attribute risk toVmorbidly obese and obese patients remains unaddressed. These inconsistencies further support the practicality of using the universally defined BMI statistic as a continuous predictor variable of complications instead of transforming this information into dichotomies for analysis. Limitations to the validity of BMI as a continuous predictor for complications in breast reconstruction include potentially abnormal predictive behavior of extreme BMI. Extremely underweight or
TABLE 5. Reoperations Due to Complications by Group Normal Weight Overweight Tissue expander 21 (9.46) explantation (%) Tissue expander exchange (%) 1 (0.45) Conversion to autologous 17 (4.05) reconstruction (%) Reconstruction failure (%) 3 (1.35)
Obese
P
20 (12.87)
23 (13.14) 0.4396
3 (1.95) 10 (7.14)
3 (1.71) 12 (9.14)
0.8138 0.5916
7 (4.55)
8 (4.57)
0.1153
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TABLE 6. Multivariate Regression of Risk Factors for Reoperation Due to Complications Odds Ratio (95% Confidence Interval)
P
V 1.0428 (1.0036Y1.0836) V V V V 0.4269 (0.2406Y0.7574)
0.1375 0.0322 0.8643 0.3067 0.3987 0.4278 0.0036
V 1.0872 (1.0014Y1.1803) V V V V V
0.6719 0.0463 0.9987 0.9988 0.9457 0.4348 0.4857
V V V V V V V
0.1109 0.9388 0.4398 0.5005 0.5550 0.4315 0.0587
V 1.0699 (1.0064Y1.1374) V V V V V
0.5192 0.0305 0.4222 0.7343 0.3029 0.4112 0.1083
Risk Factor Tissue explantation Age BMI, kg/m2 Active smoker Prior XRT Chemotherapy PXRT ADM Tissue expander exchange Age BMI, kg/m2 Active smoker Prior XRT Chemotherapy PXRT ADM Conversion to autologous reconstruction Age BMI Active smoker Prior XRT Chemotherapy PXRT ADM Reconstruction failure Age BMI, kg/m2 Active smoker Prior XRT Chemotherapy PXRT ADM
morbidly obese patients may both experience comorbidities that drastically affect surgical outcomes. Nevertheless, in those circumstances, coexisting medical concerns clearly outweigh BMI in guiding the decision to undergo reconstruction.
CONCLUSIONS This study evaluates BMI as a continuous variable predictor of complications in tissue expander-implant breast reconstructions. Stratification of patients into obese and nonobese risk groups, as is customary in the existing literature, may not adequately estimate risk for patients. By considering BMI rather than obesity, plastic surgeons may better predict outcomes and guide patient care. REFERENCES 1. Demark-Wahnefried W, Campbell KL, Hayes SC. Weight management and its role in breast cancer rehabilitation. Cancer. 2012;118(suppl 8):2277Y2287. 2. Cleary MP, Grossmann ME. Minireview: Obesity and breast cancer: the estrogen connection. Endocrinology. 2009;150:2537Y2542. 3. Calle EE, Thun MJ, Petrelli JM, et al. Body-mass index and mortality in a prospective cohort of U.S. adults. N Engl J Med. 1999;341:1097Y1105. 4. Burton BT, Foster WR, Hirsch J, et al. Health implications of obesity: an NIH Consensus Development Conference. Int J Obes. 1985;9:155Y170.
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BMI and Expander-Implant Breast Reconstructions
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Abdominoplasty, liposuction of the flanks, and obesity: analyzing risk factors for seroma formation. Plast Reconstr Surg. 2006;117:773Y781. 30. Nahas FX, Ferreira LM, Ghelfond C. Does quilting suture prevent seroma in abdominoplasty? Plast Reconstr Surg. 2007;119:1060Y1066. 31. Lin KY, Blechman AB, Brenin DR. Implant-based, two-stage breast reconstruction in the setting of radiation injury: an outcome study. Plast Reconstr Surg. 2012;129:817Y823. 32. Hirsch EM, Seth AK, Dumanian GA, et al. Outcomes of immediate tissue expander breast reconstruction followed by reconstruction of choice in the setting of post-mastectomy radiation therapy. Ann Plast Surg. 2014;72:274Y278. 33. Seth AK, Persing S, Connor CM, et al. A comparative analysis of cryopreserved versus pre-hydrated human acellular dermal matrices in tissue expander breast reconstruction. Ann Plast Surg. 2013;70:632Y635. 34. Kim JYS, Davila AA, Fine N. Breast reconstruction, dual plane expanderimplant with acellular dermal matrix. 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36. Maxwell GP, Gabriel A. Use of the acellular dermal matrix in revisionary aesthetic breast surgery. Aesthet Surg J. 2009;29:485Y493. 37. Rawlani V, Buck DW 2nd, Johnson SA, et al. Tissue expander breast reconstruction using prehydrated human acellular dermis. Ann Plast Surg. 2011;66: 593Y597. 38. Chun YS, Verma K, Rosen H, et al. Implant-based breast reconstruction using acellular dermal matrix and the risk of postoperative complications. Plast Reconstr Surg. 2010;125:429Y436. 39. Antony AK, McCarthy CM, Cordeiro PG, et al. Acellular human dermis implantation in 153 immediate two-stage tissue expander breast reconstructions:
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determining the incidence and significant predictors of complications. Plast Reconstr Surg. 2010;125:1606Y1614. 40. Sbitany H, Serletti JM. Acellular dermis-assisted prosthetic breast reconstruction: a systematic and critical review of efficacy and associated morbidity. Plast Reconstr Surg. 2011;128:1162Y1169. 41. Kim JY, Davila AA, Persing S, et al. A meta-analysis of human acellular dermis and submuscular tissue expander breast reconstruction. Plast Reconstr Surg. 2012;129:28Y41. 42. Momeni A, Ahdoot MA, Kim RY, et al. Should we continue to consider obesity a relative contraindication for autologous microsurgical breast reconstruction? J Plast Reconstr Aesthet Surg. 2012;65:420Y425.
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